Seed handling in chimpanzees (Pan troglodytes) and redtail monkeys (Cercopithecus ascanius): Implications for understanding hominoid and cercopithecine fruit-processing strategies and seed dispersal

Primates are confronted with an array of constraints in feeding on fruit, including the removal of adhesive, energy-rich pulp from seeds. In this paper, I discuss how primates meet this challenge and present data on the fruit-processing and seed-handling behavior of chimpanzees and redtail monkeys in Kibale National Park, Uganda. These data are then related to these species' services as seed dispersers. Particular attention was paid to the methods by which primates removed pulp from seeds, the density of seed clumps that they deposited (by spitting, dropping, or defecating) to the forest floor, and the distance seeds were moved from parent trees. Distance and density differences in chimpanzee and redtail seed dispersal resulted from distinct fruit-processing and seed-handling methods. It was observed, in general, that redtail monkeys engaged in fine oral processing and were seed spitters: most seeds were dispersed in close proximity to parent trees (84% of spat seeds <10 m of parent tree), and deposited singly (100% seeds spat singly). In contrast, chimpanzees were coarse fruit processors and seed swallowers: seeds were defecated in denser clumps (e.g., a mean of 149 large seeds/dung sample and hundreds of small seeds/dung sample), far from parent trees. I evaluate the factors that shape patterns of fruit processing in hominoids and cercopithecines, and argue that the observed seed handling differences can be attributed to differences in digestive retention times, oral anatomy, and alternative mechanisms by which to avoid the cost of seed ballast. Am J Phys Anthropol 109:365–386, 1999. © 1999 Wiley-Liss, Inc.     

Parasite prevalence and richness in sympatric colobines: effects of host density

Factors that influence proximity and the number and duration of contacts among individuals can influence parasite transmission among hosts, and thus parasite prevalence and species richness are expected to increase with increasing host density. To examine this prediction we took advantage of a unique situation. Following the clearing of a forest fragment that supported red colobus (Piliocolobus tephrosceles) and black-and-white colobus (Colobus guereza), the animals moved into a neighboring fragment that we had been monitoring for a number of years and for which we had described the primate parasite community. After the animals immigrated into the fragment, the colobus populations more than doubled and colobus density became almost twice that found in Kibale National Park, Uganda. Despite this increase in host density, the richness of the parasite community did not increase. However, in both colobus species the prevalence of Trichuris sp., the only commonly occurring gastrointestinal parasite, increased. Over the next 5 years the prevalence and intensity of infection of Trichuris sp. in red colobus declined and their population numbers slowly increased. In contrast, the prevalence and intensity of infection of Trichuris sp. increased in black-and-white colobus and remained high following the immigration, and their population size declined. While Trichuris sp. infections are typically asymptomatic, we consider it a possibility that they contributed to the decline of the black-and-white colobus, and that the red colobus may be serving as a reservoir for Trichuris, thereby increasing the infection risk for black-and-white colobus.     

Variation in the Nutritional Value of Primate Foods: Among Trees, Time Periods, and Areas

The study of nutritional ecology has proven to be useful for understanding many aspects of primate behavior and ecology and is a valuable tool in primate conservation. However, to date this approach has had limited application since chemical analyses of food items is very time-consuming and collections of perishable food material are often made in remote field locations. Such logistic difficulties have led to plant material being collected in a variety of fashions, and it is not known how variation in collection method might influence our understanding of the chemical basis of dietary selection. A standardization of collection methods is greatly needed to allow for direct comparison among studies. To develop an appropriate standardized method and to evaluate past research, it is necessary to understand along what dimensions plant chemistry varies. We evaluated variation in nutritional value—protein, fiber, digestibility, alkaloids, saponins, cyanogenic glycocides, and minerals—of leaf material from species eaten by red colobus (Piliocolobus tephrosceles) and black-and-white colobus (Colobus guereza) of Kibale National Park, Uganda. We consider variation at 3-levels: among trees, time periods, and areas. While there was considerable variation among species with respect to protein, digestibility, and saponins, there was also variation among individuals of the same species; in fact, individuals may vary by as much as 20%. The average coefficients of variation (CV) among individuals of the same species are 13.4 for protein, 12 for digestibility, and 43 for saponins, while the average CV among species are 35, 31.3, and 82.4, respectively. No species showed a variable response with respect to testing for the presence or absence of cyanogenic glycocides, while 2 of 11 species tested for alkaloids showed a variable response. Over 2 years there was evidence of variation among time periods in the chemical composition of the same food items. The protein-to-fiber ratio of mature leaves of the same species collected from 4 sites separated by 12 km within Kibale was also variable and in some cases the variation among sites was greater than the differences among species. For example, while Funtumia latifolia had little variation in protein-to-fiber ratio at 3 sites (0.44 at all sites), the remaining site was 28% greater. Because temporal variation is less than variation among individuals, it is likely more important to sample from multiple trees at a single point in time than to sample across time. However, the most accurate assessment of nutrient intake is obtained by collecting plant material from the specific trees selected for consumption.     

Hardness of cercopithecine foods: implications for the critical function of enamel thickness in exploiting fallback foods

We evaluate the hardness of foods consumed by sympatric Cercopithecus ascanius (redtail guenons) and Lophocebus albigena (grey-cheeked mangabeys), and consider how selection might operate to influence foraging adaptations. Since L. albigena has among the thickest dental enamel in extant primates and is commonly referred to as a hard-object consumer, we predicted that their diet would be harder than that of the guenon. Data on diet and food hardness (as measured by resistance to puncture and crushing) were collected between June-October of 1997 at Kibale National Park, Uganda, and were compared to similar data collected in Kibale between 1991-1994. Contrary to what we predicted, there was no difference in dietary hardness when the puncture resistance of all fruit consumed by the two species was compared (31 tree species in both study periods). However, in June-October 1997, L. albigena exploited a diet more resistant to puncture and crushing than C. ascanius. This difference is largely explained by the higher percentage of bark and seeds consumed by the L. albigena during this period. We suggest that it is the difference in the mechanical properties of fallback foods during critical periods that may have served as the selective pressure for thick enamel in L. albigena.     

Implications of small scale variation in ecological conditions for the diet and density of red colobus monkeys

In this 3-year investigation we documented patterns of density, diet, and activity of red colobus monkeys (Procolobus tephrosceles) in six areas in or near Kibale National Park, Uganda and related these patterns to availability of food resources. There were large differences in the density and behavior of the red colobus among the sites. For example, the red colobus at one site with a diverse plant community of more than 61 tree species, had a diet that included at least 42 species. In contrast, at a second site red colobus spent 92% of their feeding time eating from one species that dominated the tree community. The density of important red colobus food trees varied among sites from 32 trees/ha to 204 trees/ha, and red colobus density ranged from 0.70 groups/km² to 7.41 groups/km². Among sites, red colobus density was related to the cumulative DBH of important food trees, when one apparently anomalous site was excluded, and populations with more plant species in their diets tended to be those that were found at higher densities. Activity budgets of the red colobus populations varied markedly among sites. For example, feeding time ranged among sites from 29 to 55%, and traveling varied from 5 to 20%. When faced with increased foraging demands, red colobus reduced the time spent resting, while the time spent socializing remained fairly constant. Comparative socioecological studies typically contrast species separated by large geographical distances to ensure there is sufficient variation in the environment to detect behavioral responses. The marked differences in ecological conditions and red colobus behavior we documented over short geographical distances, suggests that small-scale contrasts are a useful tool to examine ecological determinants of behavior and community structure.     

Contest and Scramble Competition and the Carry-Over Effect in Globodera spp. in Potato-Based Crop Rotations Using an Extended Ricker Model

The Ricker model extended with a linear term was used to model the dynamics of a potato cyst nematode population on different potato cultivars over a wide range of population densities. The model accounts for contest and scramble competition and between-year carryover of unhatched eggs. Contest competition occurs due to the restricted amount of available root sites that are the feeding source of the female nematode. Nematodes not reaching such a feeding site turn into males and do not contribute to a new generation. Scramble competition results in a decrease of the number of eggs per cyst at high densities due to the decrease in the food supply per feeding site. At still higher densities, the size of the root system declines; then dynamics are mostly governed by carryover of cysts between subsequent years. The restricted number of three parameters in the proposed model made it possible to calculate the equilibrium densities and to obtain analytical expressions of the model''s sensitivity to parameter change. The population dynamics model was combined with a yield-loss assessment model and, using empirical Bayesian methods, was fitted to data from a 3-year experiment carried out in the Netherlands. The experiment was set up around the location of a primary infestation of Globodera pallida in reclaimed polder soil. Due to a wide range of population densities at short distances from the center of the infestation, optimal conditions existed for studying population response and damage in different cultivars. By using the empirical Bayesian methods it is possible to estimate all parameters of the dynamic system, in contrast to earlier studies with realistic biological models where convergence of parameter estimation algorithms was a problem. Applying the model to the outcome of the experiment, we calculated the minimum gross margin that a fourth crop needs to reach in order to be taken up in a 3-year rotation with potato. An equation was derived that accounted for both gross margin changes and nematode-related yield loss. The new model with its three parameters has the right level of complexity for the amount and type of collected data. Two other important models from the literature, containing five and 10 parameters respectively, may at this point turn out to be less appropriate. Consequences for research priorities are discussed and prediction schemes are taken in consideration.     

Effects of Fruit Patch Availability on Feeding Subgroup Size and Spacing Patterns in Four Primate Species at Tinigua National Park, Colombia

We examined the effects of fruit patch size, density, and distribution on feeding subgroup size and feeding bout duration in four Neotropical primates—Lagothrix lagotricha, Ateles belzebuth, Cebus apella, and Alouatta seniculus—based on 2494 hr of focal animal sampling in Tinigua National Park, Colombia. All four species show positive correlations between patch size (tree diameter at breast height; DBH) and subgroup size (maximum number of individuals from the focal group feeding at the same time), but the determination coefficients are very low and this relationship does not seem to influence strongly the actual size of the groups. Ateles showed the weakest correlation between patch size and feeding party size, and their fission–fusion sociality is best explained as a mechanism to reduce intragroup competition rather than to adjust the subgroup size to the availability of patches. Feeding associations as well as proximal spacing patterns, in general, are more alike in species with similar ecological requirements.     

Frugivory and Seed Fate in Bursera inversa (Burseraceae) at Tinigua Park,Colombia: Implications for Primate Conservation1

The large ateline primates are efficient seed dispersers in Neotropical forests and hunting is driving their populations to extinction, but we do not know whether other frugivores could substitute primates in their ecological role as seed dispersers. In this study we test this possibility using a potential keystone species (Bursera inversa) at Tinigua Park, Colombia. This plant species allows us to compare seed removal rates between emergent, isolated trees, without primate visitors and trees with connected crowns. We used traps to estimate fruit production and seed removal rates in six different trees, and fruiting trees were observed during 2 yr to quantify the number of seeds manipulated by different animal species. We carried out seed predation experiments to test if seed removal by predators was affected by distance or density effects. We found that the most productive trees attracted more visiting species and seed removal rates differed among trees, the lowest corresponding to trees without primate access. Seed removal rates from the ground by predators were not higher below parental trees than away from them, but the distribution of saplings in the forest suggests that seed dispersal is advantageous. Although it is likely that the effect of primate extinctions will vary depending on tree species traits, conserving the populations of primate seed dispersers is critical to maintain the ecological processes in this forest.